Severe drug-induced repetitive behaviors and striatal overexpression of VAChT in ChAT-ChR2-EYFP BAC transgenic mice

Frontiers in Neural Circuits

Volumn 8, Issue MAY, 2014, Pages

  Crittenden, Jill R ^a   Lacey, Carolyn J ^a   Lee, Tyrone ^a   Bowden, Hilary A ^a   Graybiel, Ann M ^a  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

Acetylcholine; Amphetamine; Dopamine; Drug addiction; Stereotypy; Striatum; Striosome

Indexed keywords

ACETYLCHOLINE; VESICULAR ACETYLCHOLINE TRANSPORTER; AMPHETAMINE; CHANNELRHODOPSIN 2, MOUSE; CHOLINE ACETYLTRANSFERASE; DOPAMINE; NICOTINIC RECEPTOR; RHODOPSIN; SLC18A3 PROTEIN, MOUSE;

ACETYLCHOLINE RELEASE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELLULAR DISTRIBUTION; CHOLINERGIC NERVE CELL; CHOLINERGIC SYSTEM; COMPULSION; CONTROLLED STUDY; CORPUS STRIATUM; LOCOMOTION; MALE; METHAMPHETAMINE DEPENDENCE; MOLECULAR PATHOLOGY; MOUSE; NEUROPIL; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; STEREOTYPY; TRANSGENIC MOUSE; ANIMAL; DRUG DEPENDENCE; DRUG EFFECT; INTERNEURON; METABOLISM; MOTOR ACTIVITY; STRIOSOME;

ACETYLCHOLINE; AMPHETAMINE; DOPAMINE; DRUG ADDICTION; STEREOTYPY; STRIATUM; STRIOSOME;

ACETYLCHOLINE; AMPHETAMINE; ANIMALS; CHOLINE O-ACETYLTRANSFERASE; CORPUS STRIATUM; INTERNEURONS; MICE; MICE, TRANSGENIC; MOTOR ACTIVITY; RECEPTORS, NICOTINIC; RHODOPSIN; STEREOTYPED BEHAVIOR; VESICULAR ACETYLCHOLINE TRANSPORT PROTEINS;

EID: 84901604220     PISSN: 16625110     EISSN: None     Source Type: Journal    
DOI: 10.3389/fncir.2014.00057     Document Type: Article

References (92)

1. Aliane, V., Perez, S., Bohren, Y., Deniau, J. M., and Kemel, M. L. (2011). Key role of striatal cholinergic interneurons in processes leading to arrest of motor stereotypies. Brain 134(Pt. 1), 110-118. doi: 10.1093/brain/awq285
2. Aliane, V., Perez, S., Nieoullon, A., Deniau, J. M., and Kemel, M. L. (2009). Cocaine-induced stereotypy is linked to an imbalance between the medial prefrontal and sensorimotor circuits of the basal ganglia. Eur. J. Neurosci. 30, 1269-1279. doi: 10.1111/j.1460-9568.2009.06907.x
3. Aosaki, T., Graybiel, A. M., and Kimura, M. (1994). Effect of the nigrostriatal dopamine system on acquired neural responses in the striatum of behaving monkeys. Science 265, 412-415. doi: 10.1126/science.8023166
4. Aosaki, T., Kimura, M., and Graybiel, A. M. (1995). Temporal and spatial characteristics of tonically active neurons of the primate's striatum. J. Neurophysiol. 73, 1234-1252.
5. Bickerdike, M. J., and Abercrombie, E. D. (1997). Striatal acetylcholine release correlates with behavioral sensitization in rats withdrawn from chronic amphetamine. J. Pharmacol. Exp. Ther. 282, 818-826. doi: 10.1016/s0920-9964(97)82197-4
6. Canales, J. J., and Graybiel, A. M. (2000). A measure of striatal function predicts motor stereotypy. Nat. Neurosci.3, 377-383. doi: 10.1038/73949
7. Capper-Loup, C., Canales, J. J., Kadaba, N., and Graybiel, A. M. (2002). Concurrent activation of dopamine D1 and D2 receptors is required to evoke neural and behavioral phenotypes of cocaine sensitization. J. Neurosci. 22, 6218-6227.
8. Chan, C. S., Peterson, J. D., Gertler, T. S., Glajch, K. E., Quintana, R. E., Cui, Q., et al. (2012). Strain-specific regulation of striatal phenotype in Drd2-eGFP BAC transgenic mice. J. Neurosci. 32, 9124-9132. doi: 10.1523/jneurosci.0229-12.2012
9. Collins, S. L., and Izenwasser, S. (2004). Chronic nicotine differentially alters cocaine-induced locomotor activity in adolescent vs. adult male and female rats. Neuropharmacology 46, 349-362. doi: 10.1016/j.neuropharm.2003.09.024
10. Crittenden, J. R., Bergmeier, W., Zhang, Y., Piffath, C. L., Liang, Y., Wagner, D. D., et al. (2004). CalDAG-GEFI integrates signaling for platelet aggregation and thrombus formation. Nat. Med. 10, 982-986. doi: 10.1038/nm1004-1139a
11. Crittenden, J. R., and Graybiel, A. M. (2011). Basal Ganglia disorders associated with imbalances in the striatal striosome and matrix compartments. Front. Neuroanat. 5:59. doi: 10.3389/fnana.2011.00059
12. Cubo, E., Fernandez Jaen, A., Moreno, C., Anaya, B., Gonzalez, M., and Kompoliti, K. (2008). Donepezil use in children and adolescents with tics and attention-deficit/hyperactivity disorder: an 18-week, single-center, dose-escalating, prospective, open-label study. Clin. Ther. 30, 182-189. doi: 10.1016/j.clinthera.2008.01.010
13. Dautan, D., Huerta-Ocampo, I., Witten, I. B., Deisseroth, K., Bolam, J. P., Gerdjikov, T., et al. (2014). A major external source of cholinergic innervation of the striatum and nucleus accumbens originates in the brainstem. J. Neurosci. 34, 4509-4518. doi: 10.1523/jneurosci.5071-13.2014
14. De La Garza, R. 2nd, Newton, T. F., Haile, C. N., Yoon, J. H., Nerumalla, C. S., Mahoney, J. J., et al. (2012). Rivastigmine reduces "Likely to use methamphetamine" in methamphetamine-dependent volunteers. Prog. Neuropsychopharmacol. Biol. Psychiatry 37, 141-146. doi: 10.1016/j.pnpbp.2011.12.014
15. Dickson, P. R., Lang, C. G., Hinton, S. C., and Kelley, A. E. (1994). Oral stereotypy induced by amphetamine microinjection into striatum: an anatomical mapping study. Neuroscience 61, 81-91. doi: 10.1016/0306-4522(94)90062-0
16. Ding, J. B., Guzman, J. N., Peterson, J. D., Goldberg, J. A., and Surmeier, D. J. (2010). Thalamic gating of corticostriatal signaling by cholinergic interneurons. Neuron 67, 294-307. doi: 10.1016/j.neuron.2010.06.017
17. Doig, N. M., Magill, P. J., Apicella, P., Bolam, J. P., and Sharott, A. (2014). Cortical and thalamic excitation mediate the multiphasic responses of striatal cholinergic interneurons to motivationally salient stimuli. J. Neurosci. 34, 3101-3117. doi: 10.1523/jneurosci.4627-13.2014
18. Doyle, J. P., Dougherty, J. D., Heiman, M., Schmidt, E. F., Stevens, T. R., Ma, G., et al. (2008). Application of a translational profiling approach for the comparative analysis of CNS cell types. Cell 135, 749-762. doi: 10.1016/j.cell.2008.10.029
19. Eblen, F., and Graybiel, A. M. (1995). Highly restricted origin of prefrontal cortical inputs to striosomes in the macaque monkey. J. Neurosci. 15, 5999-6013.
20. Eiden, L. E. (1998). The cholinergic gene locus. J. Neurochem. 70, 2227-2240. doi: 10.1046/j.1471-4159.1998.70062227.x
21. Feil, J., Sheppard, D., Fitzgerald, P. B., Yucel, M., Lubman, D. I., and Bradshaw, J. L. (2010). Addiction, compulsive drug seeking and the role of frontostriatal mechanisms in regulating inhibitory control. Neurosci. Biobehav. Rev.35, 248-275. doi: 10.1016/j.neubiorev.2010.03.001
22. Flagel, S. B., Akil, H., and Robinson, T. E. (2009). Individual differences in the attribution of incentive salience to reward-related cues: Implications for addiction. Neuropharmacology 56(Suppl. 1), 139-148. doi: 10.1016/j.neuropharm.2008.06.027
23. Fujiyama, F., Sohn, J., Nakano, T., Furuta, T., Nakamura, K. C., Matsuda, W., et al. (2011). Exclusive and common targets of neostriatofugal projections of rat striosome neurons: a single neuron-tracing study using a viral vector. Eur. J. Neurosci. 33, 668-677. doi: 10.1111/j.1460-9568.2010.07564.x
24. Fujiyama, F., Unzai, T., Nakamura, K., Nomura, S., and Kaneko, T. (2006). Difference in organization of corticostriatal and thalamostriatal synapses between patch and matrix compartments of rat neostriatum. Eur. J. Neurosci. 24, 2813-2824. doi: 10.1111/j.1460-9568.2006.05177.x
25. Gerfen, C. R., Paletzki, R., and Heintz, N. (2013). GENSAT BAC cre-recombinase driver lines to study the functional organization of cerebral cortical and basal ganglia circuits. Neuron 80, 1368-1383. doi: 10.1016/j.neuron.2013.10.016
26. Gerfen, C. R. (1984). The neostriatal mosaic: compartmentalization of corticostriatal input and striatonigral output systems. Nature 311, 461-464. doi: 10.1038/312172a0
27. Gong, S., Doughty, M., Harbaugh, C. R., Cummins, A., Hatten, M. E., Heintz, N., et al. (2007). Targeting Cre recombinase to specific neuron populations with bacterial artificial chromosome constructs. J. Neurosci. 27, 9817-9823. doi: 10.1523/jneurosci.2707-07.2007
28. Gong, S., Zheng, C., Doughty, M. L., Losos, K., Didkovsky, N., Schambra, U. B., et al. (2003). A gene expression atlas of the central nervous system based on bacterial artificial chromosomes. Nature 425, 917-925. doi: 10.1038/nature02033
29. Gonzales, K. K., Pare, J. F., Wichmann, T., and Smith, Y. (2013). GABAergic inputs from direct and indirect striatal projection neurons onto cholinergic interneurons in the primate putamen. J. Comp. Neurol. 521, 2502-2522. doi: 10.1002/cne.23295
30. Goto, Y., Otani, S., and Grace, A. A. (2007). The Yin and Yang of dopamine release: a new perspective. Neuropharmacology 53, 583-587. doi: 10.1016/j.neuropharm.2007.07.007
31. Grando, S. A., Kawashima, K., Kirkpatrick, C. J., and Wessler, I. (2007). Recent progress in understanding the non-neuronal cholinergic system in humans. Life Sci. 80, 2181-2185. doi: 10.1016/j.lfs.2007.03.015
32. Graybiel, A. M., Baughman, R. W., and Eckenstein, F. (1986). Cholinergic neuropil of the striatum observes striosomal boundaries. Nature 323, 625-627. doi: 10.1038/323625a0
33. Graybiel, A. M., Moratalla, R., and Robertson, H. A. (1990). Amphetamine and cocaine induce drug-specific activation of the c-fos gene in striosome-matrix compartments and limbic subdivisions of the striatum. Proc. Natl. Acad. Sci. U S A 87, 6912-6916. doi: 10.1073/pnas.87.17.6912
34. Graybiel, A. M. (2008). Habits, rituals and the evaluative brain. Annu. Rev. Neurosci. 31, 359-387. doi: 10.1146/annurev.neuro.29.051605.112851
35. Graybiel, A. M., and Ragsdale, C. W. Jr. (1978). Histochemically distinct compartments in the striatum of human, monkeys and cat demonstrated by acetylthiocholinesterase staining. Proc. Natl. Acad. Sci. U S A 75, 5723-5726. doi: 10.1073/pnas.75.11.5723
36. Grybko, M. J., Hahm, E. T., Perrine, W., Parnes, J. A., Chick, W. S., Sharma, G., et al. (2011). A transgenic mouse model reveals fast nicotinic transmission in hippocampal pyramidal neurons. Eur. J. Neurosci. 33, 1786-1798. doi: 10.1111/j.1460-9568.2011.07671.x
37. Heiman, M., Schaefer, A., Gong, S., Peterson, J. D., Day, M., Ramsey, K. E., et al. (2008). A translational profiling approach for the molecular characterization of CNS cell types. Cell 135, 738-748. doi: 10.1016/j.cell.2008.10.028
38. Herkenham, M., and Pert, C. B. (1981). Mosaic distribution of opiate receptors, parafascicular projections and acetylcholinesterase in rat striatum. Nature 291, 415-418. doi: 10.1038/291415a0
39. Horner, K. A., Hebbard, J. C., Logan, A. S., Vanchipurakel, G. A., and Gilbert, Y. E. (2012). Activation of mu opioid receptors in the striatum differentially augments methamphetamine-induced gene expression and enhances stereotypic behavior. J. Neurochem 120, 779-794. doi: 10.1111/j.1471-4159.2011.07620.x
40. Horner, K. A., and Keefe, K. A. (2006). Regulation of psychostimulant-induced preprodynorphin, c-fos and zif/268 messenger RNA expression in the rat dorsal striatum by mu opioid receptor blockade. Eur. J. Pharmacol. 532, 61-73. doi: 10.1016/j.ejphar.2005.12.041
41. Inokawa, H., Yamada, H., Matsumoto, N., Muranishi, M., and Kimura, M. (2010). Juxtacellular labeling of tonically active neurons and phasically active neurons in the rat striatum. Neuroscience 168, 395-404. doi: 10.1016/j.neuroscience.2010.03.062
42. Jedynak, J. P., Cameron, C. M., and Robinson, T. E. (2012). Repeated methamphetamine administration differentially alters fos expression in caudate-putamen patch and matrix compartments and nucleus accumbens. PLoS One 7:e34227. doi: 10.1371/journal.pone.0034227
43. Jimenez-Castellanos, J., and Graybiel, A. M. (1989). Evidence that histochemically distinct zones of the primate substantia nigra pars compacta are related to patterned distributions of nigrostriatal projection neurons and striatonigral fibers. Exp. Brain Res. 74, 227-238. doi: 10.1007/bf00248855
44. Jog, M. S., Kubota, Y., Connolly, C. I., Hillegaart, V., and Graybiel, A. M. (1999). Building neural representations of habits. Science 286, 1745-1749. doi: 10.1126/science.286.5445.1745
45. Karler, R., Calder, L. D., and Bedingfield, J. B. (1996). A novel nicotinic-cholinergic role in behavioral sensitization to amphetamine-induced stereotypy in mice. Brain Res. 725, 192-198. doi: 10.1016/s0006-8993(96)00248-x
46. Kawaguchi, Y. (1992). Large aspiny cells in the matrix of the rat neostriatum in vitro: physiological identification, relation to the compartments and excitatory postsynaptic currents. J. Neurophysiol. 67, 1669-1682.
47. Kawaguchi, Y. (1993). Physiological, morphological and histochemical characterization of three classes of interneurons in rat neostriatum. J. Neurosci. 13, 4908-4923.
48. Kawasaki, H., Springett, G. M., Toki, S., Canales, J. J., Harlan, P., Blumenstiel, J. P., et al. (1998). A Rap guanine nucleotide exchange factor enriched highly in the basal ganglia. Proc. Natl. Acad. Sci. U S A 95, 13278-13283. doi: 10.1073/pnas.95.22.13278
49. Kincaid, A. E., and Wilson, C. J. (1996). Corticostriatal innervation of the patch and matrix in the rat neostriatum. J. Comp. Neurol. 374, 578-592. doi: 10.1002/(sici)1096-9861(19961028)374:4<578::aid-cne7>3.3.co;2-i
50. Kolisnyk, B., Al-Onaizi, M. A., Hirata, P. H., Guzman, M. S., Nikolova, S., Barbash, S., et al. (2013a). Forebrain deletion of the vesicular acetylcholine transporter results in deficits in executive function, metabolic and RNA splicing abnormalities in the prefrontal cortex. J. Neurosci. 33, 14908-14920. doi: 10.1523/jneurosci.1933-13.2013
51. Kolisnyk, B., Guzman, M. S., Raulic, S., Fan, J., Magalhaes, A. C., Feng, G., et al. (2013b). ChAT-ChR2-EYFP mice have enhanced motor endurance but show deficits in attention and several additional cognitive domains. J. Neurosci. 33, 10427-10438. doi: 10.1523/jneurosci.0395-13.2013
52. Kramer, P. F., Christensen, C. H., Hazelwood, L. A., Dobi, A., Bock, R., Sibley, D. R., et al. (2011). Dopamine D2 receptor overexpression alters behavior and physiology in Drd2-EGFP mice. J. Neurosci. 31, 126-132. doi: 10.1523/jneurosci.4287-10.2011
53. Kuczenski, R., and Segal, D. S. (2001). Caudate-putamen and nucleus accumbens extracellular acetylcholine responses to methamphetamine binges. Brain Res. 923, 32-38. doi: 10.1016/s0006-8993(01)03193-6
54. Lanciego, J. L., Gonzalo, N., Castle, M., Sanchez-Escobar, C., Aymerich, M. S., and Obeso, J. A. (2004). Thalamic innervation of striatal and subthalamic neurons projecting to the rat entopeduncular nucleus. Eur. J. Neurosci. 19, 1267-1277. doi: 10.1111/j.1460-9568.2004.03244.x
55. Langer, L. F., and Graybiel, A. M. (1989). Distinct nigrostriatal projection systems innervate striosomes and matrix in the primate striatum. Brain Res. 498, 344-350. doi: 10.1016/0006-8993(89)91114-1
56. Lapper, S. R., and Bolam, J. P. (1992). Input from the frontal cortex and the parafascicular nucleus to cholinergic interneurons in the dorsal striatum of the rat. Neuroscience 51, 533-545. doi: 10.1016/0306-4522(92)90293-b
57. Liao, W. L., Tsai, H. C., Wang, H. F., Chang, J., Lu, K. M., Wu, H. L., et al. (2008). Modular patterning of structure and function of the striatum by retinoid receptor signaling. Proc. Natl. Acad. Sci. U S A 105, 6765-6770. doi: 10.1073/pnas.0802109105
58. Matsuda, W., Furuta, T., Nakamura, K. C., Hioki, H., Fujiyama, F., Arai, R., et al. (2009). Single nigrostriatal dopaminergic neurons form widely spread and highly dense axonal arborizations in the neostriatum. J. Neurosci.29, 444-453. doi: 10.1523/jneurosci.4029-08.2009
59. Matsumoto, N., Minamimoto, T., Graybiel, A. M., and Kimura, M. (2001). Neurons in the thalamic CM-Pf complex supply striatal neurons with information about behaviorally significant sensory events. J. Neurophysiol. 85, 960-976.
60. Metaxas, A., Keyworth, H., Yoo, J., Chen, Y., Kitchen, I., and Bailey, A. (2012). The stereotypy-inducing and OCD-like effects of chronic 'Binge' cocaine are modulated by distinct subtypes of nicotinic acetylcholine receptors. Br. J. Pharmacol. 167, 450-464. doi: 10.1111/j.1476-5381.2012.02023.x
61. Minamimoto, T., Hori, Y., and Kimura, M. (2009). Roles of the thalamic CM-PF complex-Basal ganglia circuit in externally driven rebias of action. Brain Res. Bull. 78, 75-79. doi: 10.1016/j.brainresbull.2008.08.013
62. Miura, M., Masuda, M., and Aosaki, T. (2008). Roles of micro-opioid receptors in GABAergic synaptic transmission in the striosome and matrix compartments of the striatum. Mol. Neurobiol. 37, 104-115. doi: 10.1007/s12035-008-8023-2
63. Morris, G., Arkadir, D., Nevet, A., Vaadia, E., and Bergman, H. (2004). Coincident but distinct messages of midbrain dopamine and striatal tonically active neurons. Neuron 43, 133-143. doi: 10.1016/j.neuron.2004.06.012
64. Murray, R. C., Gilbert, Y. E., Logan, A. S., Hebbard, J. C., and Horner, K. A. (2013). Striatal patch compartment lesions alter methamphetamine-induced behavior and immediate early gene expression in the striatum, substantia nigra and frontal cortex. Brain Struct. Funct. doi: 10.1007/s00429-013-0559-x. [Epub ahead of print].
65. Nagy, P. M., and Aubert, I. (2012). Overexpression of the vesicular acetylcholine transporter increased acetylcholine release in the hippocampus. Neuroscience 218, 1-11. doi: 10.1016/j.neuroscience.2012.05.047
66. Nair, V. P., and Hunter, J. M. (2004). Anticholinesterases and anticholinergic drugs. Contin. Educ. Anaesth. Crit. Care Pain 4, 164-168. doi: 10.1093/bjaceaccp/mkh045
67. Perez, X. A., O'Leary, K. T., Parameswaran, N., McIntosh, J. M., and Quik, M. (2009). Prominent role of alpha3/alpha6beta2* nAChRs in regulating evoked dopamine release in primate putamen: effect of long-term nicotine treatment. Mol. Pharmacol. 75, 938-946. doi: 10.1124/mol.108.053801
68. Raju, D. V., Shah, D. J., Wright, T. M., Hall, R. A., and Smith, Y. (2006). Differential synaptology of vGluT2-containing thalamostriatal afferents between the patch and matrix compartments in rats. J. Comp. Neurol. 499, 231-243. doi: 10.1002/cne.21099
69. Ren, J., Qin, C., Hu, F., Tan, J., Qiu, L., Zhao, S., et al. (2011). Habenula "cholinergic" neurons co-release glutamate and acetylcholine and activate postsynaptic neurons via distinct transmission modes. Neuron 69, 445-452. doi: 10.1016/j.neuron.2010.12.038
70. Reynolds, J. N., and Wickens, J. R. (2004). The corticostriatal input to giant aspiny interneurons in the rat: a candidate pathway for synchronising the response to reward-related cues. Brain Res. 1011, 115-128. doi: 10.1016/j.brainres.2004.03.026
71. Rossi, J., Balthasar, N., Olson, D., Scott, M., Berglund, E., Lee, C. E., et al. (2011). Melanocortin-4 receptors expressed by cholinergic neurons regulate energy balance and glucose homeostasis. Cell Metab. 13, 195-204. doi: 10.1016/j.cmet.2011.01.010
72. Sadikot, A. F., Parent, A., Smith, Y., and Bolam, J. P. (1992). Efferent connections of the centromedian and parafascicular thalamic nuclei in the squirrel monkey: a light and electron microscopic study of the thalamostriatal projection in relation to striatal heterogeneity. J. Comp. Neurol. 320, 228-242. doi: 10.1002/cne.903200207
73. Saka, E., Goodrich, C., Harlan, P., Madras, B. K., and Graybiel, A. M. (2004). Repetitive behaviors in monkeys are linked to specific striatal activation patterns. J. Neurosci. 24, 7557-7565. doi: 10.1523/jneurosci.1072-04.2004
74. Saka, E., Iadarola, M., Fitzgerald, D. J., and Graybiel, A. M. (2002). Local circuit neurons in the striatum regulate neural and behavioral responses to dopaminergic stimulation. Proc. Natl. Acad. Sci. U S A 99, 9004-9009. doi: 10.1073/pnas.132212499
75. Sarter, M., Parikh, V., and Howe, W. M. (2009). Phasic acetylcholine release and the volume transmission hypothesis: time to move on. Nat. Rev. Neurosci. 10, 383-390. doi: 10.1038/nrn2635
76. Schindelin, J., Arganda-Carreras, I., Frise, E., Kaynig, V., Longair, M., Pietzsch, T., et al. (2012). Fiji: an open-source platform for biological-image analysis. Nat. Methods 9, 676-682. doi: 10.1038/nmeth.2019
77. Schneider, C. A., Rasband, W. S., and Eliceiri, K. W. (2012). NIH Image to ImageJ: 25 years of image analysis. Nat. Methods 9, 671-675. doi: 10.1038/nmeth.2089
78. Schultz, W. (2007). Multiple dopamine functions at different time courses. Annu. Rev. Neurosci. 30, 259-288. doi: 10.1146/annurev.neuro.28.061604.135722
79. Schulz, J. M., Oswald, M. J., and Reynolds, J. N. (2011). Visual-induced excitation leads to firing pauses in striatal cholinergic interneurons. J. Neurosci. 31, 11133-11143. doi: 10.1523/jneurosci.0661-11.2011
80. Siegal, D., Erickson, J., Varoqui, H., Ang, L., Kalasinsky, K. S., Peretti, F. J., et al. (2004). Brain vesicular acetylcholine transporter in human users of drugs of abuse. Synapse 52, 223-232. doi: 10.1002/syn.20020
81. Song, H., Ming, G., Fon, E., Bellocchio, E., Edwards, R. H., and Poo, M. (1997). Expression of a putative vesicular acetylcholine transporter facilitates quantal transmitter packaging. Neuron 18, 815-826. doi: 10.1016/s0896-6273(00)80320-7
82. Tappe, A., and Kuner, R. (2006). Regulation of motor performance and striatal function by synaptic scaffolding proteins of the Homer1 family. Proc. Natl. Acad. Sci. U S A 103, 774-779. doi: 10.1073/pnas.0505900103
83. Thomsen, M., and Caine, S. B. (2011). Psychomotor stimulant effects of cocaine in rats and 15 mouse strains. Exp. Clin. Psychopharmacol. 19, 321-341. doi: 10.1037/a0024798
84. Threlfell, S., and Cragg, S. J. (2011). Dopamine signaling in dorsal versus ventral striatum: the dynamic role of cholinergic interneurons. Front. Syst. Neurosci. 5:11. doi: 10.3389/fnsys.2011.00011
85. Threlfell, S., Lalic, T., Platt, N. J., Jennings, K. A., Deisseroth, K., and Cragg, S. J. (2012). Striatal dopamine release is triggered by synchronized activity in cholinergic interneurons. Neuron 75, 58-64. doi: 10.1016/j.neuron.2012.04.038
86. Ting, J. T., and Feng, G. (2014). Recombineering strategies for developing next generation BAC transgenic tools for optogenetics and beyond. Front. Behav. Neurosci. 8:111. doi: 10.3389/fnbeh.2014.00111
87. Watabe-Uchida, M., Zhu, L., Ogawa, S. K., Vamanrao, A., and Uchida, N. (2012). Whole-brain mapping of direct inputs to midbrain dopamine neurons. Neuron 74, 858-873. doi: 10.1016/j.neuron.2012.03.017
88. Witten, I. B., Steinberg, E. E., Lee, S. Y., Davidson, T. J., Zalocusky, K. A., Brodsky, M., et al. (2011). Recombinase-driver rat lines: tools, techniques and optogenetic application to dopamine-mediated reinforcement. Neuron 72, 721-733. doi: 10.1016/j.neuron.2011.10.028
89. Yin, H. H., Mulcare, S. P., Hilario, M. R., Clouse, E., Holloway, T., Davis, M. I., et al. (2009). Dynamic reorganization of striatal circuits during the acquisition and consolidation of a skill. Nat. Neurosci. 12, 333-341. doi: 10.1038/nn.2261
90. Zhang, H., and Sulzer, D. (2012). Regulation of striatal dopamine release by presynaptic auto-and heteroreceptors. Basal Ganglia 2, 5-13. doi: 10.1016/j.baga.2011.11.004
91. Zhao, S., Ting, J. T., Atallah, H. E., Qiu, L., Tan, J., Gloss, B., et al. (2011). Cell type-specific channelrhodopsin-2 transgenic mice for optogenetic dissection of neural circuitry function. Nat. Methods 8, 745-752. doi: 10.1038/nmeth.1668
92. Zhou, F. M., Liang, Y., and Dani, J. A. (2001). Endogenous nicotinic cholinergic activity regulates dopamine release in the striatum. Nat. Neurosci. 4, 1224-1229. doi: 10.1038/nn769